Under a changing climate, cultivating climate-resilient crops will be critical to maintaining food security. Here, we propose the application of reactive oxygen species (ROS)-generating nanoparticles as nanobiostimulants to trigger stress/immune responses and subsequently increase the stress resilience of plants. We established three regimens of silver nanoparticles (AgNPs)-based "stress training": seed training (ST), leaf training (LT), and combined seed and leaf training (SLT). Trained rice seedlings were then exposed to either rice blast fungus (Magnaporthe oryzae) or chilling stress (10 °C). The results show that all "stress training" regimes, particularly SLT, significantly enhanced the resistance of rice against the fungal pathogen (lesion size reduced by 82% relative to untrained control). SLT also significantly enhanced rice tolerance to cold stress. The mechanisms for the enhanced resilience were investigated with metabolomics and transcriptomics, which show that "stress training" induced considerable metabolic and transcriptional reprogramming in rice leaves. AgNPs boosted ROS-activated stress signaling pathways by oxidative post-translational modifications of stress-related kinases, hormones, and transcriptional factors (TFs). These signaling pathways subsequently modulated the expression of defense genes, including specialized metabolites (SMs) biosynthesis genes, cell membrane lipid metabolism genes, and pathogen-plant interaction genes. Importantly, results showed that the "stress memory" can be transferred transgenerationally, conferring offspring seeds with improved seed germination and seedling vigor. This may provide an epigenetic breeding strategy to fortify stress resilience of crops. This nanobiostimulant-based stress training strategy will increase yield vigor against a changing climate and will contribute to sustainable agriculture by reducing agrochemical use.
Keywords: climate resilience; immune memory; nanobiotechnology; nanozyme; rice; rice blast; stress memory.